Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops

Abstract

Background: Global annual losses in agricultural production from salt-affected land are in excess of US$12 billion and rising. At the same time, a significant amount of arable land is becoming lost to urban sprawl, forcing agricultural production into marginal areas. Consequently, there is a need for a major breakthrough in crop breeding for salinity tolerance. Given the limited range of genetic diversity in this trait within traditional crops, stress tolerance genes and mechanisms must be identified in extremophiles and then introduced into traditional crops.

Scope and conclusions: This review argues that learning from halophytes may be a promising way of achieving this goal. The paper is focused around two central questions: what are the key physiological mechanisms conferring salinity tolerance in halophytes that can be introduced into non-halophyte crop species to improve their performance under saline conditions and what specific genes need to be targeted to achieve this goal? The specific traits that are discussed and advocated include: manipulation of trichome shape, size and density to enable their use for external Na(+) sequestration; increasing the efficiency of internal Na(+) sequestration in vacuoles by the orchestrated regulation of tonoplast NHX exchangers and slow and fast vacuolar channels, combined with greater cytosolic K(+) retention; controlling stomata aperture and optimizing water use efficiency by reducing stomatal density; and efficient control of xylem ion loading, enabling rapid shoot osmotic adjustment while preventing prolonged Na(+) transport to the shoot.

Keywords: Salinity; cytosolic potassium; drought; epidermal bladder; membrane potential; osmotic adjustment; sodium sequestration; stomata; trichome; vacuole; xylem loading.

Fig. 1.

The effect of salinity on growth and biomass accumulation of (A) halophyte (quinoa; Chenopodium quinoa ‘5206’) and (B) non-halophyte (wheat; Triticum durum ‘Towner’) species. Optimal quinoa growth is observed at NaCl concentrations between 100 and 200 mm, while wheat growth is highly suppressed by 150 mm NaCl. The photogrpah in (A) is reproduced from Hariadi et al. (2011), with permission from the Society for Experimental Botany. The photograph in (B) is courtesy of Dr Tracey Ann Cuin.

Fig. 2.

Micrograph of trichomes (A, B) and salt bladders (C, D) on the abaxial surface of two glycophyte (arabidopsis and barley) and two halophyte (quinoa and Atriplex) species. Images were taken using a scanning electron microscope in environmental mode. Phototographs are courtesy of Dr Jayakumar Bose (TIA) and Dr Karsten Goemann (Central Science Laboratory), University of Tasmania.

Fig. 3.

The decrease in stomatal density under saline conditions correlates positively with relative plant yield. Relative changes (% control) in stomatal density were measured in barley and quinoa (as indictaed in the key) genotypes contrasting in salinity tolerance. These are plotted against relative shoot biomass (% control; fresh weight basis). Numbers next to the letter Q indicate specific quinoa varieties, as in Shabala et al. (2013).

Fig. 4.

A hypothetical model depicting the kinetics of xylem loading and the mechanisms involved. At initial (control) conditions (A), cytosolic Na⁺ concentrations in xylem parenchyma cells are low, and the membrane potential is too negative to allow passive xylem Na⁺ loading via non-selective cation channels (NORCs). Active Na⁺ transporters are not constitutively expressed so do not contribute to the process. The onset of salinity stress results in a substantial depolarization of root cells (Wegner et al., 2011), accompanied by the progressive accumulation of Na⁺ in the parenchyma cell cytosol, while the xylem Na⁺ concentration remains low. This enables channel-mediated xylem Na⁺ loading (B). As Na⁺ is loaded in the xylem, the xylem Na⁺ concentration becomes higher, and parenchyma cells also become repolarized, making further passive loading impossible. Further xylem Na⁺ loading may be mediated by one of two active transport systems: either SOS1 (Na⁺/H⁺ exchanger) or CCC (2Cl⁻:Na⁺:K⁺ symporter) (C). Depending on whether these transporters are constitutively expressed or are inducible by salinity, the kinetics of xylem Na⁺ will differ significantly.